Pergamon
J. therm. Eiol. Vol. 20. No. 112. DD.61-74. 1995
Copyright 0 1995 Else&r Science Ltd
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0306_4565(94)ooo28-x
EFFECTS OF TEMPERATURE
ON THE SIZE OF AQUATIC
ECTOTHERMS: EXCEPTIONS TO THE GENERAL RULE
DAVID ATKINSQN
Population
Biology Research Group, Department of Environmental and Evolutionary Biology,
University of Liverpool, P.O. Box 147, Liverpool L69 3BX, U.K.
Abstract-l.
Of 61 studies of aquatic ectotherms, increased rearing temperature (apparently not stressful
for growth and development) caused a reduction in organism size at a given developmental stage in 55
cases (90.2%) and an increase in only six (9.8%).
2. The six exceptions to the size-reduction rule included one diatom (Phaeoductylum tricornutum), one
copepod (Sulmincola salmoneus) and four species of mayfly (Ephemeroptera). The extent to which these
exceptions could be explained by each of four mechanisms was investigated by comparing their life cycles
and niches with those of other closely-related species.
3. No satisfactory explanation could be found for the response of P. tricornutum, but mechanisms
consistent with the response of S. sulmoneus were: reduced risk of oxygen shortage, low risk of ectotherm
predation and seasonal constraints on the life cycle. The latter may also help explain the four mayfly
exceptions.
Key Word Index: Temperature; body size, life history; ectotherms; growth; Ephemeroptera;
Salmincola salmoneus; Bacillariophyta; Phaeodactylum tricornutum; phenotypic plasticity
INTRODUCTION
Copepoda;
1994). No single overriding physiological constraint
or adaptive explanation has yet been found to
account for the general size reduction.
One approach to identifying the causes of major
variation in the temperature-size relationship is to
compare life cycles and niches of species which are
exceptions to the general rule with those of species
which follow the rule, especially species which are
otherwise closely related taxonomically and ecologically. This paper focuses on published phenotypic
plasticity in organism size, rather than genetic variation related to temperature differences. Re-examination of existing data may not provide definitive
explanations but can help narrow the range of hypotheses to be tested. Here, I consider the extent to
which exceptions to the general rule from aquatic
environments that have been reported in the literature can be explained by each of four mechanisms
that relate temperature to size-at-stage. Any combination of the four mechanisms may operate on a
given population.
of a smaller adult body at increased
The production
rearing temperatures is easily explicable if temperatures are stressfully high or resources are either in
short supply or of poor quality so that individual
growth rates are reduced (Brett, 1971; Cossins and
Bowler, 1987; Moore and Folt, 1993). A more
difficult problem is to explain why an organism’s size
at a given developmental stage should be reduced by
increased rearing temperatures under conditions with
abundant resources and when the temperature increase is observed or expected to increase an individual’s growth rate. Yet this reduction in size has been
observed in over 80% of ectotherms studied, including members of the Protista, four phyla and eight
classes of animal, two families of plant and one
bacterium species-from
terrestrial and aquatic
habitats (Atkinson, 1994). Earlier studies broadly
support this finding (Bclehridek, 1935; Ray, 1960;
von Bertalanffy, 1960; Precht ef al., 1973).
Temperature can affect organism size at a given
developmental stage by constraining growth (von
Bertalanffy, 1960; Atkinson, 1994) or by altering
the adaptive value of body size (Loosanoff, 1959;
Culver, 1980; Roff, 198 1; Myers and Runge, 1986;
Chrzanowski et al., 1988; Atkinson, 1994) or of
developmental
rate (Myers and Runge, 1986;
Atkinson, 1994; Atkinson, 1995; Sibly and Atkinson,
Mechanism
limitation for
1:
Oxygen
Iimitation
Increased temperature both
of dissolved oxygen in water
increases respiratory activity
for oxygen. According to this
61
(carbon
dioxide
autotrophs)
reduces the amount
(Wilber, 1964) and
and hence demand
mechanism, even if
62
DAVID ATKINSON
individual growth rate is not immediately reduced at
high temperatures, high temperatures may still correlate with future oxygen shortage in the organism’s
natural environment. For autotrophs, when nutrient
and light levels are high, the amount of dissolved
carbon dioxide (CO,) may become limiting (e.g.
Fogg, 1965). In either case, temperature could thus
act as a cue for future risks, and hence alter the
optimal time to mature (Atkinson, 1994; Sibly and
Atkinson, 1994). All else being equal, exceptions to
the general temperature-size
rule would thus be
expected to come from environments in which high
temperature was not normally associated with future
shortage of oxygen (or CO2 for autotrophs).
Mechanism 2: Habitat loss
For some habitats such as small seasonal ponds
and streams, increased evaporation at increased temperatures can increase the likelihood of their drying
out. Again, therefore, for organisms adapted to these
habitats temperature might serve as a cue for future
risks, and hence alter the optimal time to mature
(Atkinson, 1994; Sibly and Atkinson, 1994), or to
produce forms capable of either resisting desiccation
or allowing dispersal to sites with more favourable
conditions. According to this mechanism, exceptions
to the general temperature-size rule would be more
likely to come from environments not prone to
desiccation at high temperatures rather than from
ones that sometimes dried out.
Mechanism 3: Risk of predation by other ectotherms
Using adaptationist reasoning, many authors have
predicted that, all else being equal, increased juvenile
mortality should favour earlier maturation at a
smaller size (Williams, 1966; Wilbur and Collins,
1973; Roff, 1981; Werner, 1986; Ludwig and Rowe,
1990; Rowe and Ludwig, 1991; Kawecki and Stearns,
1993; Sibly and Atkinson, 1994). Feeding rates of
ectotherm predators generally increase with increasing non-stressful temperature whilst endotherm predation may even be reduced (Atkinson, 1994). Thus,
for organisms that mainly experience ectotherm predation, an increased temperature may serve as a cue
for increased predation risks and hence favour earlier
maturation even at the expense of time spent growing. I propose that among the species least likely to
experience ectotherm predation
are very large
species-at least during the latter part of their development when they are protected by their large size.
Increased temperature would be less likely to favour
reduced adult size in these species than in those with
higher predation risks.
A complicating factor is the possibility of sizedependent predation. For instance, in small plank-
tonic species, small size can provide protection from
size-selective ectothermic predators such as fish and
large insects (Zaret, 1980; Dodson, 1989; Stibor and
Liming, 1994). This advantage of small size has been
proposed to explain the general size reduction in
some planktonic species at increased temperature
(Culver, 1980; Chrzanowski et al., 1988). Conversely,
some invertebrate predators of planktonic species
prefer small individuals (Zaret, 1980; Stibor and
Ltining, 1994). Data on size-selective predation are
likely to be unavailable for the majority of populations for which temperature effects on size are
known. In the present paper, therefore, I just consider
whether exceptions to the general temperature-size
rule include very large species.
Mechanism 4: Seasonal effects
Many organisms mature at particular times of year
and use photoperiod as a seasonal cue (e.g. Masaki,
1978; Tauber et al., 1986; Roberts and Summerfield,
1987; Nyhn et al., 1989; Ellis et al., 1990; Scott and
Dingle, 1990). In organisms reared under photoperiods that indicate that little time would normally
be available in their natural environment before
maturity must be reached (e.g. before food would
normally deteriorate) faster juvenile growth at increased temperatures could lead to the production of
larger rather than smaller adults since those from all
temperature treatments would mature at similar
times (or photoperiods). According to this mechanism, exceptions to the general rule would be found in
species which must pass a particular developmental
stage at a particular time of year and which are reared
in the laboratory under photoperiods near to those at
which the particular developmental event normally
occurs.
MATERIALS AND METHODS
Published studies of the effects of rearing temperature on size-at-stage of aquatic ectotherms were
examined. Whilst some genetic evolution during the
experiments may have been unavoidable in species
with very short generation times (e.g. protists, bacteria), the rapidity of response even in some of these
suggests that phenotypic plasticity was also observed
(e.g. Margalef, 1954). The criteria for inclusion of
studies in the review are summarized here and
discussed more fully by Atkinson (1994).
In those studies deemed acceptable for inclusion,
environmental conditions were controlled and the
range of temperatures allowed the organisms to reach
maturity but did not attain values so stressfully high
that an increase was shown to reduce rates of individual growth or differentiation. Temperatures that were
63
Temperature and size of aquatic ectotherms
obviously outside the range normally encountered by
the species were also excluded as were temperatures
so low that daily mortality rate was increased with
reduced temperature, despite a presumed lower metabolic rate. Also studies were excluded if there was
evidence that the amount of resources were limiting
or the food provided was both unnatural and caused
a reduction in growth rate below that on other foods.
However, most studies lacked at least some relevant
data (e.g. growth rates, photoperiod, food quality).
Quality of data is taken into account in the analysis
of exceptions to the general rule in the present paper.
The review focused on studies of developmental
stages near to reproductive maturity. In unicells,
however, size at initiation of fission was only available from one study (Adolph, 1929). Therefore, to
increase sample size of protists, less precise measures
such as average size over a period of several generations were also included. Size measures included dry
or wet weights, or correlates of organism weight such
as body length or exoskeletal dimensions. Finally,
only experiments in which statistically significant
(P < 0.05) effects of temperature on size had been
found (by the authors or myself) were included in the
review.
The present paper extends the preliminary work of
Atkinson (1994) by examining the extent to which
exceptions to the general rule can be explained by
mechanisms 14. The following information was
sought from published sources for those species for
which the relevant mechanism was applicable:
(1) Evidence that any oxygen (or CO,) limitation
at high temperatures in the natural environment would be less than for other related
aquatic species in the review (mechanism 1);
(2) Evidence for an association
between increased temperature and habitat drying out
(mechanism 2);
(3) Organism size (mechanism 3);
(4) Evidence of an association between a particular
stage of the life history and a particular time of
year (mechanism 4). [It was not possible, however, to identify the extent to which juvenile
developmental
period was constrained
by
season.]
RESULTS
Sixty-one studies of aquatic organisms satisfied the
criteria for inclusion in the review (Table 1). The
organisms included one bacterium, seven protists
(five autotrophic, two heterotrophic), two rotifers,
four molluscs, twenty-six insects, thirteen crustaceans, seven amphibians and one fish (Table 1).
Whilst most species were from freshwater, eight were
from saltwater environments.
Fifty-five studies (90.2%) showed a size reduction
with increased rearing temperature, whilst only six
(9.8%) showed a size increase (Table 1). These six
exceptions to the general rule, described below, comprised one protist (Fawley, 1984), one copepod crustacean (Johnston and Dykeman, 1987), and four
mayflies (Sweeney and Vannote, 1978; Vannote and
Sweeney, 1980).
Exception 1: Phaeodactylum
tricornutum
(Bacillario-
pbta)
At high light intensities, cell width and volume of
this pennate marine diatom increased with each increase in rearing temperature over five treatments
Table 1. Summary by taxon of effects of increased rearing temperature on aquatic organism size
Kingdom
Monera
(Bacteria)
Protists
Animalia
Phylum
Chlorophyta
Bacillariophyta
Ciliophora
Aschelminthes
Mollusca
Arthropoda
Class
Total
No. of reductions
No. of increases
0
0
Rotifera
Gastropoda
Pelecypoda
Insecta
Crustacea
Chordata
Sub-class/Order
(for Arthropoda)
Diptera
Ephemeroptera
Copepoda
Decapoda
Mysidacea
Amphibia
Osteichthyes
55
DAVID ATKINSON
64
from
14 to 23”C-a
population
range
growth
and
considered
1984). At lower light intensities
resource
limitation
became less pronounced
for
(Fawley,
there was the risk of
but on that of the fish host.
and the in-
data),
and kelts are typically
in temperature
gradually
Paton
and Dunlop,
with declining light intensity.
temperature
the size of the parasite
The Atlantic salmon kelts, measured to the tail fork,
were 68-72cm
long (C. E. Johnston,
unpublished
the results,
affecting
crease in size with increase
Increased
optimal
photosynthesis
increased
the rate of carbon-
2-6 kg in weight
1898). They are therefore
the largest organisms
of the sixty-one
review (Appendix),
to have major risks of predation
up to 23°C. [A 25°C treatment-apparently
Consequently,
for rate
of development-was
excluded
from
the
creased
an increased
temperatures
present review]. To reduce the risks of other variables
selection
affecting
at the expense
the interpretation
of the results,
iments
used enriched
artificial
seawater
tained
a 14:lO hour
1ight:dark
regime
(Fawley,
and mainthroughout
freshwater
chlorophytes
increased
temperatures
is available
algae in this review were
and had reduced cell sizes at
(Appendix).
organisms
any association
between
and oxygen or CO* limitation
infor-
conditions
were adapted,
high temperature
or habitat
1 and 2). Mechanism
(mechanisms
Little
on the environmental
to which the experimental
including
Whilst
drying out
3 and 4 do not
“advanced
of light period
March.
thereafter.
several generations
a particular
developmental
with a particular
Exception 2: Salmincola
length
pod, which was reared
stage is not
time of year.
pear to interact
in this parasitic
on gills of Atlantic
salmon
thought
1987).
The other five species of copepod were free-living and
each showed size reductions with increased temperature (Table 2). S. salmoneus was the only gill parasite
present in the sample of 61 studies in the review, and
uniquely
supply modified
in this review, have had an
by fish respiratory
This suggests the possibility
sation by the fish at increased
tain
4) apMore-
(1941)
on salmon
between
another
only
that respiratory
compen-
temperatures,
to main-
between
life-history
1989). These
and
results
of the other
by Abdullahi
Laybourn-Parry
throughout
differ
shortage
for
(mechanism
requirements
the parasite
at increased
1). However, the oxygen
of S. salmoneus were not
a strong
and
those
time of
et nl.,
for at least
studied
and
Laybourn-Parry
et al. (1988)
which
to
were
(1985)
reproduce
the year (Table 2).
Exceptions 3-6: Four mayjy species (Ephemeroptera)
Whilst five mayfly species had a reduced dry weight
at adult emergence
at increased
temperatures,
despite
faster
growth
and development
(Sweeney
Vannote,
1978, 1984; Vannote and Sweeney,
Sweeney et al., 1986; Soderstrom,
temperatures
consumption
a
in the re-
copepods
had an increased
of oxygen
stage
from
may
the
parasites
and time of
of the copepods
risks
entering
adult
adulthood
gills,
of oxygen
S. salmoneus
kelts by May, suggesting
reduce, prevent or delay any increased
amounts
normally
activity.
in
naturally
waters and spawns in the late winter (McLaren
three
oxygen
day length
was maintained
year: it has a strictly annual life cycle in Nova Scotia
lower temperatures
would therefore,
day length
view, Pseudocalanus minutus, also shows
cope-
and Dykeman,
from short day length
(summer)
with the effect of temperature.
by Friend
association
an
in which the length
effects (mechanism
association
(Salmo salar) kelts under simulated
natural daylengths, was significantly greater at higher than at
(Johnston
simulated
were kept under
over, at least in the life cycle of Scottish
strong
even
effects were ob-
to 21 June and then declined
year. However,
(Copepoda)
salmoneus
(body)
per week,
was increased
Thus seasonal
were present
trunk
size under
regime”
This maximum
described
Adult
affected
to the longest
from March
strong
of the parasite,
no significant
photoperiod
in January
at in-
to provide
of size at the time of maturity.
temperature
size, can pass through
associated
is unlikely
photoperiods,
apply to these species since they are of microscopic
and therefore
by other ectotherms.
for rapid development
natural
in this
risk of predation
served when fish and parasites
1984).
The other four unicellular
mation
the exper-
included
and hence one of the least likely
fixation per cell per hour, and the rate of cell division
stressful
(e.g.
easily
1988) another
dry weight (Sweeney,
and
1980;
four
1978; Sweeney
and Vannote,
1978; Vannote and Sweeney, 1980).
The recent discovery of a second species of Zsonychia
measured to allow this idea to be tested. Other factors
that may affect the importance of oxygen shortage are
in the study stream of White Clay Creek (I. Circe),
whose small larvae closely resemble those of I. bicolor
(B. W. Sweeney, unpublished
data) suggests that
considered in the Discussion.
No information
on any association
the data on Isonychiu (Sweeney, 1978) may refer to
two species. These species have different life cycles
between
high
temperature
and the drying up of the salmon kelt
rivers (mechanism 2) is known.
In this example, any size-related protection
from
ectothermic
predation
(mechanism
3) depends
not on
(B. W. Sweeney, unpublished data; Table 3). [Other
species and experimental
treatments
studied
by
these authors
were not included
in the review
since they either lacked size differences
between
Reduced
Increased
Pseudocalanus minutus
Salmincola salmoneus
‘Effect of increased temperature
on size-at-stage.
‘Size measurements
are means from the treatments
Johnston/Dykeman).
Reduced
Macrocyclops albidus
Reduced
Reduced
Reduced
(syn. Cyclops viridis)
Cy-
Cyclops serrulalus
A. viridis
Acanihocyclops vernalis (syn.
elops vernalis)
Species
Temperature
on size’
of lakes, esp. eutrophic
the largest
Atlantic
in
sizes; weights
salmon
of lakes, esp. eutrophic
plankton
Gills of
freshwater
Marine
Benthos
ones
size’
reproductive
reproductive
Spawns
reproductive
in late winter
throughout
throughout
(Abdullahi/Laybourn-Parry),
lengths
(1933)
and
Abdullahi
and
(1985);
e/ al. (1988)
Abdullahi
(1985)
(Coker,
(1987);
(1970);
Lock/McLaren,
Johnston and Dykeman
Friend (1941)
Lock
and McLaren
McLaren et al. (1989)
Abdullahi and Laybourn-Parry
(1985); Laybourn-Parry
er al.
(1988)
Coker
Coker (1933);
Laybourn-Parry
Laybourn-Parry
Coker (1933);
Laybourn-Parry
References
are body lengths
Altered daylength
regime prevents
temperatureesize
response;
only
adults found by May in Scottish
population
Univoltine;
Probably
year
(No information)
Probably
year
Probably
year
throughout
in six species of Copepod
Association
of dev.
stage with time of vr
characteristics
4.82 mm (host probably > 70 cm long 26 kg wt)
1.01 mm
44pg
1.32mm
53 fig
3Opg
1.62 mm
Organism
and life-cycle
are fresh weights
and selected habitat
of lakes, esp. eutrophic
(No information)
Benthos
ones
Benthos
ones
Habitat
relationships
and sex producing
effect
Table 2. Temperature-size
g
2
8
6
b
g
R
g
8.
6
a
5
d
B
a
2
%
9.5 mm
10.5 mm
0.5 mg
15.9 mg
1.72 mg
4.42 mg
Reduced
Reduced
Increased
Increased
Increased
Increased
Caenis simulans
Isonychia bicolor4
atratus
funeralis
P. chelifer
Tricorythodes
Eurylophella
funeralis)
Univoltine; a winter-spring species
Egg diapause April-August
3 + generations/yr; expt. used 13: 11
LD regime and offspring of overwintering generation.
Univoltine; no egg diapause observed; adults emerge late March
Univoltine; emergence typically in
June
Univoltine; emergence typically in
June
Possible
egg diapause
September-May; a summer species
Bivoltine in White Clay Creek; summer generation examined
Possible egg diapause
September-May; a summer species
Univoltine in White Clay Creek; no
egg diapause; a winter-spring species
Association of developmental
stage with time of year’
Vannote
Sweeney
Vannote
Sweeney
and Sweeney (1980); B. W.
(unpublished)
and Sweeney (1980); B. W.
(unpublished)
Sweeney et al. (1986); B. W. Sweeney
(unpublished)
Siiderstrom (1988); Siiderstriim and
Johansson (1988)
Siiderstriim (1988); Siiderstrijm and
Johnansson (1988)
Vannote and Sweeney (1980); B. W.
Sweeney (unpublished)
Sweeney (1978)
Vannote and Sweeney (1980); B. W.
Sweeney (unpublished)
Sweeney and Vannote (1984)
References
‘Effect of increased temperature on size-at-stage.
*Size measurements are those in the treatments and sex producing the largest sizes; weights are dry weights (Sweeney/Vannote); lengths are body lengths (Soderstrom).
3Larvae of “winterspring”
species hatch from eggs in the autumn but grow mainly during winter and spring; in “summer” species most growth and resource exploitation
is from May to September.
%tudy may have included specimens of Zsonychia Circe which has a short summer generation and probably egg diapause from September to May (B. W. Sweeney, unpublished).
(syn. Ephemerella
minor
Parameletus
3.70 mg
Reduced
intermedia
Leptophlebia
1.8mg
Reduced
triangulifer (syn. Cloeon tri-
3.85 mg
Reduced
Ameletus ludens
Centroptilum
angulifer)
Organism size*
Temperature effect
on size’
relationships and life-cycle characteristics in nine species of mayfly (Ephemeroptera)
Species
Table 3. Temperature-size
Temperature and size of aquatic ectotherms
that I was able to demonstrate were
significantly different (P < 0.05), grew slower at
increased temperatures, or were provided with food
of demonstrably inadequate quality]. In the work by
Sweeney and Vannote, both cooling and warming,
relative to ambient stream temperature of White
Clay Creek, Pennsylvania, usually produced a reduction in size of emerging adults, which supported
their concept of a thermal optimum at which body
size and fecundity were maximal. Eurylophellu
funeralis, however, showed the opposite response
(i.e. increased size) when temperature was raised
above ambient (Table 4 in Vannote and Sweeney,
1980).
No direct evidence is presented by Sweeney and
Vannote to indicate that oxygen limitation (mechanism 1) at increased temperatures was greater for some
of the study species from White Clay Creek than for
others. However, exceptions to the general rule (excluding E. funeralis) were found among species or
generations whose growth was confined mainly to
the summer months of May to September, when
mean stream temperatures were high, whereas those
which followed the general rule grew mainly during
the winter and spring (Sweeney and Vannote,
1978; Vannote and Sweeney, 1980; Table 3). High
summer temperatures may lead to a reduction in
oxygen content of the stream water. According to
mechanism 1, an oxygen shortage at increased temperatures in summer, rather than in winter or spring,
would favour rapid maturation and small adult size
particularly in the summer-reared mayflies. Yet the
increase in size of “summer” species at increased
temperature runs counter to this prediction. However, neither the oxygen content of the water in the
experiments nor the oxygen consumption requirements of the different species at different temperatures are known, and therefore any suggestion that
mechanism 1 is unimportant
in explaining the
variation amongst the mayfly species must still be
provisional.
Since the likelihood of drought will be highest
during the summer months, selection for rapid maturity (and smaller size) would be predicted under
mechanism 2 especially for “summer” species at
increased temperatures. The fact that mayflies from
White Clay Creek reared during the summer (and
subject to natural summer photoperiods; B. W.
Sweeney, unpublished data) attained larger, not
smaller, sizes when reared at increased temperatures
(Table 3) suggests that mechanism 2 is not the
primary ultimate cause of the differences observed
among these species. However, two species of
Parameletus, which produced smaller adults at increased temperature (Sdderstrdm, 1988) were from
temperatures
61
habitats including seasonal streams that in some
years dried out causing major population losses
(Soderstriim and Johansson, 1988).
The species that were exceptions to the general
rule were not significantly different in size from
those from the same river which showed size reductions at increased temperature (T = 12, P > 0.1,
Mann-Whitney test; Table 3) so there is no evidence
that size-related protection from ectotherm predators
(mechanism 3) caused the different responses to
temperature.
The contrasting size responses to increased temperature between species growing mainly during the
summer and those growing mainly during the winter
and spring (Table 3) might be explicable if emergence
had to be more synchronized around a particular
time of year in the “summer” species or generations
than in the “winter-spring”
species or generations
(mechanism 4). No information is available to me on
whether emergence is more synchronized around a
particular time of year in the “summer” species or
generations.
DISCUSSION
A general rule
The reduction in size at a given developmental stage
observed at increased rearing temperatures in 90.2% of
studies occurred despite the exclusion from the review
of studies and treatments in which growth rates were
observed or expected to be reduced, rather than
increased, with increasing temperature. It is of course
possible that certain examples would turn out to be
inadmissible if experimental protocols and effects on
growth and mortality had been more fully recorded.
Effects of gaps in the data set on the proportion of size
reductions have been analyzed by Atkinson (1994) and
found not to alter the general result.
The proportion of aquatic ectotherms showing a
reduced size-at-stage when reared at increased temperatures is greater than the proportion found among
terrestrial species, but not significantly so (P > 0.2;
Atkinson, 1994). In the absence of known fundamental physiological constraints on growth and size at the
increased temperatures
(Atkinson,
1994) explanations have recently been proposed which consider
the optimal developmental period and adult size
when temperature correlates with mortality and
population growth as well as individual growth (Sibly
and Atkinson, 1994). The four mechanisms proposed
in the present paper to try to explain the occurrence
of aquatic exceptions to the general rule relate environmental temperature to risks of increased mortality or reduced future growth. The extent to which
68
these mechanisms
discussed next.
DAVID ATKINSON
may explain the exceptions
are
Photosynthetic protists
Why was Phaeodactylum tricornutum but not the
four other algal examples an exception to the general
rule? The review provided insufficient information to
allow evaluation of possible explanations.
Information on individual growth rate of cells at
the different temperatures was not available for
Scenedesmus obliquus (Margalef, 1954) or for the
three species of Chlamydomonas (Ray, 1960),
although rates of Chlamydomonas cell division did
increase with increasing temperature (Ray, 1960). In
Phaeodactylum tricornutum at high light intensities,
increased temperatures up to 23°C increased rate of
carbon-fixation
per cell and rate of cell division
(Fawley, 1984). Since cell size was increased too,
growth rate per cell was presumably increased. Therefore, only for P. tricornutum was there evidence for
increasing growth rates at increased temperatures.
Hence the possibility that the other species were
cultured under conditions which reduced growth with
increasing temperature-inadmissible
as examples illustrating the general temperature-size rule+annot
be ruled out.
Effects of energy supply (light intensity) on algae
can complicate the interpretation
of temperature
effects on size in a way not found in studies of
heterotrophs. Unlike heterotrophs whose growth is
not limited by energy supply if excess high quality
food is provided, individual algal growth is limited
not only by low light intensities (insufficient energy),
but also by very high light intensities. Moreover, the
high light intensity at which growth retardation starts
to occur can increase with increasing temperature, as
was found in the cryptophyte Cryptomonas erosa
(Morgan and Kalff, 1979). Thus for some species it
may be impossible to find a single light intensity that
will enable them to grow at each of several temperatures without energy supply limiting growth in at
least one of them.
Fawley (1984) related his results to the observation
that P. tricornutum thrives in light-limited, poorlymixed mass-culture systems at temperatures below
20°C and are rarely found above this temperature.
Increased cell size was associated with increased
chloroplast size, especially at low light intensities, and
both of these generally increase sinking rate (Eppley
et al., 1967; Walsby and Reynolds, 1980; Fawley,
1984). Thus a rapid rate of sinking at high temperature would reduce the abundance of the alga at least
from near the water surface.
Whilst cell division is often inhibited at extremely
high temperatures, resulting in the production of
large cells (Lloyd et al., 1982) cell division was
observed to accelerate with increasing temperature up
to 23°C in P. tricornutum, thereby precluding this
explanation. No other physiological constraints permitting large P. tricornutum cell sizes only at increased temperatures are known to the author. Nor
is the adaptive significance of increased sinking rates
at high temperatures clear, especially in open water
where cells could be completely removed from the
euphotic zone. If increased sinking rate was an
adaptive response to stressful conditions then the
stress at these higher temperatures
and light
conditions was not seen as reduced rates of cell
growth and division. No data were available to
test if mortality rates were increased with increased
temperature.
Studies not included in the Appendix-because
of
risks of light intensities inhibiting growth only at
certain temperatures, or possible genetic adaptation
to the experimental treatments, or lack of significant
effects of temperature-contained
two species which
followed the general temperature-size rule (Morgan
and Kalff, 1979; Meeson and Sweeney, 1982) and two
species whose sizes were not significantly affected by
temperature (Yoder, 1979; Meeson and Sweeney,
1982).
In conclusion, further research is required to establish the extent to which photosynthetic protists follow
the temperature-size
rule described by Atkinson
(1994). Satisfactory explanations are also still required for the relationships so far observed between
temperature and cell size.
Copepods
At least three of the four mechanisms-oxygen
limitation, ectotherm predation risk and need to
complete particular life-cycle stages by particular
times of year--could help explain why the gill parasite Salmincola salmoneus was the only exception
among thirteen crustacean studies (Tables 1 and 2).
No information is available to allow mechanism
2-the risk of habitat drying out-to
be rejected.
Other mechanisms, besides or instead of respiratory compensation by the salmon, may reduce the
risk of oxygen shortage for S. salmoneus. Atlantic
salmon, which have a high oxygen requirement,
appear in nature to avoid conditions with low
levels of dissolved oxygen (Priede et al., 1988). Moreover, since the parasitic copepod is sedentary, it is
unlikely to have a high respiratory demand and is
therefore unlikely to suffer oxygen shortage at the
oxygen concentrations experienced while the host
remains alive. Further studies on gill parasites,
especially when compared with non-gill parasites on
the same fish would help identify how important, if
Temperature and size of aquatic ectotherms
at all, are fish gills in affecting the size response to
temperature.
It has now been well established that selection
pressures from size-specific predation can be powerful
enough to cause phenotypically plastic changes in life
history in aquatic ectotherms including crustacea.
Stibor and Liming (1994) for example, showed that
waterborne cues released by predators that prefer
large adults of the cladoceran Duphnia hyalinn caused
the daphnids to reproduce at a smaller size whereas
cues released from predators preferring small juvenile
D. hyalinu caused reproduction at increased size.
Phenotypically plastic shifts in adult size due to
differences in predation risk at different temperatures
have not yet been studied.
Indirect evidence was found to support the idea
that seasonal constraints force S. sulmoneus to complete maturation before a particular time of year
(mechanism 4). The strength of these constraints
could not be ascertained but the fact that a change in
photoperiod can remove the effect of increasing temperature on size suggests that further investigation of
this phenomenon would be worthwhile.
Muyflies
Only one of the mechanisms-an
association between life-history stage and time of year-showed the
predicted relationship between temperature and size.
Generally, exceptions to the temperature-size rule
were confined to species whose growth occurred
mainly during the summer months. But information
on whether dates of emergence for these “summer”
species were under greater constraint than for those
for “winter-spring” species is not known. Moreover,
Eurylophellu funeralis proves an exception to this
relationship since it was a “winter-spring”
species
which produced larger adults at increased temperatures.
An alternative explanation is provided by Sweeney
and Vannote (1978) and Vannote and Sweeney (1980)
who applied the concept of an optimal thermal
regime to mayfly populations. This regime was typically found in rivers near the latitudinal centre of the
species’ geographic range, and maximized adult size
and fecundity. Thus for species whose geographic
range approximately centred on White Clay Creek
(WCC), maximal adult size was generally found at
ambient WCC temperatures. These authors account
for the increased size of E. jiinerulis at temperatures
higher than WCC by noting that this species has a
more southern distribution than the others (Sweeney
and Vannote, 1978) and thus is adapted to waters
warmer than WCC. The concept of an optimal
thermal regime is thus capable of explaining all
the mayfly exceptions to the general rule shown in
69
Table 3. However, it is also evident from these studies
that the optimal thermal regime for maximizing adult
size is usually cooler than that which maximizes
individual growth rate (Vannote and Sweeney, 1980;
Atkinson, 1994).
If the ambient thermal regime generally produces
maximal adult size in mayfhes, to what extent might
this explain temperature-size relationships in other
taxa in this review? Rempel and Carter (1987) found
that temperatures higher than ambient produced
smaller adult dipterans, which is consistent with both
the idea of the optimal thermal regime and the
general temperature-size rule. Other studies generally
used fixed temperatures and constant rather than
naturally varying photoperiods, but at least one
found that reductions in size with increased temperature were only observed at the upper end of the range
of temperatures normally encountered in nature
(Nayar, 1969). Another even found that a size increase was observed with increasing temperature at
the lower end of the range, at the bottom of which
mortality was also particularly high (Johns, 1981). If
we expect the optimal thermal regime to be at
temperatures away from extremes of the range normally encountered in nature, these examples appear
to support the idea of the optimal thermal regime.
Yet many others do not. In these others the range of
temperatures over which a significant reduction in
size was observed was the full range of temperatures
stated by the authors to be normally encountered by
the population in nature (Lock and McLaren, 1970;
Pourriot,
1973; Abdullahi and Laybourn-Parry,
1985; Marian and Pandian, 1985; Chrzanowski et al.,
1988; Laybourn-Parry
et al., 1988; Hanazato and
Yasuno, 1989). I suggest that the association between
ambient water temperature and maximal adult size
found by Sweeney and Vannote should apply to
species in which the timing of maturation is tightly
constrained by season and under conditions (e.g.
photoperiods) which indicate these constraints to the
growing organism. The tighter these constraints the
more likely is synchronous maturation among treatments expected and an increased size in individuals at
higher temperatures due to their faster growth. For
species adapted to conditions warmer than the ambient conditions at a particular site (e.g. Eurylophellu
funeralis above) these time constraints are likely to be
particularly acute. These constraints would be relaxed in species normally less constrained by season,
or if photoperiods indicate plenty of time is available
to complete juvenile development. In these cases,
factors that have been predicted to produce the
general size reduction at increased temperatures
could make delayed maturation and larger size in
the slower growing individuals reared at lower
DAVID ATKINSON
70
temperatures adaptive. These factors include increased risks of mortality or reduced future growth
at increased temperature-associated
with faster
ageing, more ectotherm predation, risks of oxygen
shortage or habitat drying (Atkinson, 1994; Sibly
and Atkinson, 1994).
In conclusion, the small number of aquatic exceptions to the widespread temperature-size rule observed in ectotherms belong to three main taxonomic
groups. Whilst rigorous tests of mechanisms that
might explain these exceptions were not possible
using existing published data, a comparison of life
cycles and niches among exceptions and non-exceptions to the rule that were otherwise closely related
taxonomically and/or ecologically enabled me to
highlight those mechanisms worthy of further investigation. This was particularly helpful in the identification of mechanisms
likely to produce the
exceptional response to temperature by the parasitic
copepod. Salmincola salmoneus and in four mayflies
species.
Acknowledgements--I
thank C. E. Johnston
and B. W.
Sweeney for providing
comments
and additional
information about their studies of S. salmoneus and mayflies,
respectively. An anonymous referee suggested an alternative
mechanism that would prevent exposure of S. salmoneus to
low oxygen levels at high temperatures.
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APPENDIX
Effects of Increased Temperature on Size-at -stage
R denotes significant (P < 0.05) size reduction; I denotes a significant size increase. Criteria for acceptance
of studies are given in the Materials and Methods.
No.
KINGDOM
PHYLUM
Class
(Sub Class/Order)
Species
Effect
Reference
BACI’ERIA
(MONERA)
1
Pseudomonas sp.
R
Chrzanowski et al. (1988)
R
R
R
R
Ray (1960)
Ray (1960)
Ray (1960)
Margalef (1954)
I
Fawley (1984)
R
R
Adolph (1929)
Ray (1960)
R
R
Pourriot (1973)
Lebedeva and Gerasimova (1985)
R
R
Pechenik (1984)
Imai (1937)
PROTISTA
Chlamydomonas reinhardi
Chlamydomonas sp. 1
Chlamydomonas sp. 2
Scenedesmus obliquus
BACILLARIOPHYTA
6
7
8
Phaeodactylum lricornurum
CILIOPHORA
Colpoda sp.
Terrahymena gelei
ANIMALIA
ASCHELMINTHES
Rotifera
Brachionus calycifiorus
Philodina roseola
MOLLUSCA
Gastropoda
Crepidula fornicala
Lymnaea japonica
Pelecypoda
Temperature and size of aquatic ectotherms
13
Appendix-continued
No.
13
14
KINGDOM
PHYLUM
Class
(Sub Class/Order)
Species
Effect
Reference
Mytilus edulis
R
Pechenik et al. (1990)
M edulis
R
Bayne (1965)
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
I
R
I
I
R
R
R
I
Rempel and Carter (1987)
van den Heuvel(l963)
Galliard and Golvan (1957)
Brust (1967)
Marks (1954)
Nayar (1969)
Brust (1967)
Hanazato and Yasuno (1989)
Rempel and Carter (1987)
Nayar (1968)
Mullens and Rutz (1983)
Akey et al. (1978)
Brust (1967)
Rempel and Carter (1987)
Rempel and Carter (1987)
Rempel and Carter (1987)
Rempel and Carter (1987)
Vannote and Sweeney (1980)
Vannote and Sweeney (1980)
Sweeney and Vannote (1984)
Vannote and Sweeney (1980)
Sweeney (1978)
Sweeney et al. (1986)
Siiderstriim (1988)
Siiderstriim (1988)
Vannote and Sweeney (1980)
R
R
R
R
R
R
R
R
R
I
Coker (1933)
Abdullahi and Layboum-Parry (1985)
Abdullahi and Laybourn-Parry (1985)
Coker (1933)
Laybourn-Parry et al. (1988)
Coker (1933)
Abdullahi and Layboum-Parry (1985)
Laybourn-Parry et al. (1988)
Lock and McLaren (1970)
Johnston and Dykeman (1987)
R
R
Lefler (1972)
Johns (1981)
R
Johnston and Northcote (1989)
R
R
R
Harkey and Semlitsch (1988)
Smith-Gill and Berven (1979)
Ray (1960)
ARTHROPODA
Insecta
(Diptera)
15
16
17
18
19
20
21
22
23
24
25
26
21
28
29
30
31
32
33
34
35
36
31
38
39
40
Ablabesmyia mallochi
Aedes aegypti
Ae. aegypti
Ae. nigromaculis
Ae. pseudoscutellaris
Ae. taeniorhyncus
Ae. vexans
Chaoborus jlavicans
Conchapelopia aleta
Culex nigripalpus
Culicoides variipennis
C. variipennis
Culiseta inornata
Nilotanypus jimbriatus
Parametriocnemus lundecki
Polypedihun aviceps
Stempeilinella brevis
Ameletus ludens
Caenis simulans
Cloeon triangulifer
Ephemerella funeralis
Isonychia bicolor
Leptophlebia intermedia
Parameletus minor
P. chelifer
Tricorythodes atratus
Crustacea
(Copepoda)
41
42
43
44
45
46
41
48
49
50
Acanthocyclops vernalis
A. vernalis
A. viridis
A. viridis
A. viridis
Cyclops serrulatus
Macrocyclops albidus
M. albidus
Pseudocalanus minutus
Salmincola salmoneus
(Decapoda)
51
52
Callinectes sapidus
Cancer irroratus
(Mysidacea)
53
Neomysis mercedis
CHORDATA
Amphibia
54
55
56
Pseudoacris ornata
Rana pipiens
R. sylvatica
continued-
74
DAVID ATKINSON
Appendix-continued
KINGDOM
PHYLUM
Class
(Sub Class/Order)
No.
57
58
59
60
61
R.
R.
R.
R.
sylvatica
sylvatica
sylvatica
tigrina
Osteichthyes
Paralichthys olivaceus
Species
Reference
Effect
R
R
R
R
Berven and Gill (1983)
Berven and Gill (1983)
Berven and Gill (1983)
Marian and Pandian (1985)
R
Seikai
e-tal. (1986)